Abstract
Helicobacter pylori infection remains a major global health problem, particularly in resource-limited settings, and is a leading cause of several gastrointestinal diseases. This study aimed to determine the prevalence of H. pylori seropositivity and its associated factors, including mode of delivery, among asymptomatic adolescents in Central Sudan. A community-based cross-sectional study was conducted between April and May 2025. Sociodemographic data, anthropometric measurements, and mode of delivery were collected using a structured questionnaire. H. pylori seropositivity was assessed using a rapid antibody test detecting H. pylori-specific antibodies. Univariate and multivariate binary logistic regression analyses were performed to identify associated factors. A total of 235 adolescents were enrolled, of whom 124 (52.8%) were males. The overall prevalence of H. pylori seropositivity was 24.7%. Univariate analysis showed that mode of delivery was the only factor significantly associated with H. pylori seropositivity. This association remained significant in multivariate analysis (adjusted odds ratio = 3.97; 95% confidence interval: 1.04–15.18), indicating a higher risk among adolescents delivered by cesarean section. Other factors, including age, sex, body mass index, family size, parental education and occupation, and displacement status, were not significantly associated. H. pylori positivity is relatively common among asymptomatic adolescents in Central Sudan. The use of a rapid serological antibody test represents an important limitation because it cannot distinguish between active infection and previous exposure. Consequently, the reported prevalence more accurately reflects H. pylori seropositivity than confirmed active infection. Mode of delivery may represent an important early-life risk factor, underscoring the need for further longitudinal research.
Keywords: Helicobacter pylori, adolescent, age, prevalence, cesarean section, Sudan
1. Introduction
Helicobacter pylori (H. pylori) is a Gram-negative bacterium with a helical shape that colonises the gastric mucosa of humans, affecting approximately half of the world’s population [1]. Infection with H. pylori is a primary cause of several diseases, including chronic gastritis, peptic ulcer disease, gastric adenocarcinoma, and mucosa-associated lymphoid tissue (MALT) lymphoma [2–5]. The global spread of H. pylori places a significant burden on health systems, particularly in poor healthcare settings such as those in Africa, including Sudan [6,7]. A recent estimate indicates that Africa had the highest pooled prevalence of H. pylori infection (70.1%) compared to other regions [7]. H. pylori infection remains highly prevalent in children and adolescents worldwide [8]. While there is a decreasing trend in the prevalence of H. pylori infection in children globally, the overall prevalence in African countries remains high (at 70%) [4]. Understanding the trend of H. pylori infection in children and adolescents is essential for predicting its related diseases, including gastric cancer in later life [4,9]. H. pylori infection in children and adolescents has been linked to various extra-gastric pathologies, such as iron deficiency anaemia [10–12], growth retardation, and diabetes mellitus [12]. The World Health Organisation (WHO) defines adolescence as the phase of life between childhood and adulthood, typically between the ages of 11 and 19 years [13]. This period is crucial in human development and an important time for establishing the foundations for good health [13].
The prevalence of H. pylori varies significantly across geographical regions, with higher rates observed in low- and middle-income countries (LMICs). This is often attributed to socioeconomic factors, poor sanitation, and crowded living conditions [4,5]. Transmission routes for H. pylori are primarily faecal–oral, oral–oral, or gastro–oral, and infection is often acquired in childhood, persisting throughout life if left untreated [5].
Different prevalence rates of H. pylori infection have been reported in children and adolescents in various populations in Africa [2,14–19], including 65.7% in Ethiopia [14], 32.8% in the South-Western region of Nigeria [17], and 59.7% in Port Harcourt Metropolis, Nigeria [2]. For example, a study of 402 adolescents aged 10 to 18 years revealed a high prevalence of H. pylori infection (59.7%), which was attributed to the poor hygiene practices of the adolescents and their low educational level [2].
Furthermore, numerous risk factors have been reported to be associated with H. pylori in children and adolescents, including sex [15,16], age [14,18], household size [19], parental education and employment [2,19,20], and body mass index (BMI) [21].
Increased awareness, appropriate screening, early identification, and individualised treatment approaches for H. pylori during early childhood and adolescence are recommended as preventive measures to avoid complications [9]. These preventive strategies are particularly necessary in African contexts, such as Sudan, where resources are limited. Furthermore, according to the WHO, adolescents make up more than 20% of the population in Sudan [22].
Adolescents are a critical age group for studying H. pylori epidemiology. While many infections are asymptomatic, understanding the prevalence and risk factors in this population is crucial for public health purposes. This information can help inform strategies for prevention and early intervention to reduce the long-term burden of H. pylori-related diseases [4,9–12,23]. In Sudan, like in many other LMICs, the exact burden of H. pylori infection, particularly among asymptomatic community-dwelling adolescents, is not well-studied [24]. Existing studies often focus on symptomatic patients or specific children or adult populations, leaving a significant knowledge gap regarding community-level prevalence and associated factors in younger age groups, specifically adolescents [25,26].
One interesting area of research concerns the potential role of early life events, such as mode of delivery, in shaping an individual’s susceptibility to H. pylori infection. While short-term risks associated with caesarean section for mother, baby, and subsequent pregnancies have received more attention, less focus has been on the long-term risks [27–31]. The high global prevalence rate of caesarean sections necessitates exploration of all risks, including the long-term ones [27–31]. The mode of delivery (vaginal vs. caesarean section) is known to influence the initial colonisation of the newborn gut microbiome, which in turn can impact immune development and susceptibility to various infections [32,33]. Several studies have explored the association between the mode of delivery and health conditions such as respiratory tract infections, asthma, allergies, and overweight/obesity in offspring [27–31]. However, these studies recognised infections as a long-term consequence of caesarean section, with less focus on specific infectious agents. For example, a recent systematic review and meta-analysis revealed a consistent association between caesarean section birth and a greater risk of hospital admission with respiratory and gastrointestinal infections in children across various settings [29]. The association with H. pylori acquisition remains less explored, particularly in high-prevalence settings such as Sudan.
Vaginal birth exposes newborns to the mother’s vaginal and faecal microbiota, which is crucial for the initial colonisation of the infant gut with beneficial bacteria [27,34,35]. By contrast, caesarean-section births are associated with a distinct microbial colonisation pattern, often characterised by reduced diversity and a higher abundance of skin-associated bacteria [27,34,35]. This altered early microbial environment in infants delivered via caesarean section might render them more susceptible to H. pylori colonisation or less equipped to clear the infection, possibly due to differences in immune programming or gut barrier function [27,34,35]. Therefore, the present study aimed to investigate the prevalence and associated factors, including adolescents’ mode of delivery, of H. pylori seropositivity in asymptomatic adolescents (aged 10 to 19 years) residing in Central Sudan. By identifying these factors, the study seeks to contribute to a better understanding of H. pylori seropositivity in a vulnerable population and potentially uncover previously unrecognised risk factors relevant for public health interventions.
2. Methods
2.1. Study design and setting
This community-based cross-sectional study was conducted from April to June 2025 among adolescents in Central Sudan. The study took place in Elrikieb, East Gezira, located in east-central Sudan between the Blue and White Nile rivers. Elrikieb was selected because it consists of four sub-villages whose inhabitants are representative of Gezira State as a whole. Throughout this study, the authors closely followed the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) guidelines [36].
2.2. Study population and sampling
A total of 235 adolescents were recruited for the study. A multi-stage stratified random sampling approach was employed to select participants. Within each selected sub-village, households were chosen randomly using the lottery method, and the number of households was proportional to the sub-village population. One adolescent from each eligible household was invited to participate (using the lottery method). If the household refused to participate or if there was no adolescent, the next household was chosen.
Before data collection, informed consent was obtained from parents and guardians. The definition of adolescents was based on the WHO’s definition [22]. Therefore, all adolescents aged 10 to 19 years were included in the study, while those younger or older were excluded. Participants who did not provide consent were also excluded. All the participants recruited were apparently healthy; those who were sick or pregnant, as well as nursing adolescent girls, were excluded from the study.
2.3. Data collection
After the adolescents and their guardians signed an informed consent form, the selected adolescents were surveyed. Sociodemographic data were collected using a questionnaire, including age (in years), sex (male or female), number of family members, parental educational level (<secondary or ≥ secondary), mother’s employment status (housewife or employed), father’s employment status (employed [self-employed, private, or government] or unemployed), and tobacco use by the adolescent (yes or no). The adolescent’s mode of delivery was noted (vaginal or caesarean section). Anthropometric measurements, such as weight and height, were taken using standard procedures. Finally, BMI was calculated as weight (kg)/height (m)2.
2.4. Processing of blood samples
In sterile conditions, each participant provided 3–5 ml of blood for H. pylori serology testing. The blood samples were centrifuged at 1,500 rpm for 15 minutes, and an H. pylori antibody test was performed following the manufacturer’s instructions (Hangzhou All Test Biotech Co., Ltd., China, REF: HP-302). The H. pylori antibody rapid test is a quick visual immunoassay for detecting specific IgM and IgG antibodies to H. pylori. Widely used, this test has high sensitivity and specificity [14] and was previously utilised in Sudan [24]. In this study, the authors classified the results as either positive or negative for H. pylori seropositivity.
2.5. Sample size calculation
A total of 235 adolescents were recruited to participate in the study. The authors assumed that 16% of the adolescents would be seropositive for H. pylori, based on published work among adolescents in northern Sudan, where the prevalence was 10% [24]. Due to the displacement conditions, the authors assumed that a higher rate of H. pylori was present among adolescents (16%). The sample size of 235 adolescents was calculated to detect a difference of 5% at α = 0.05, with a power of 80%. The authors also accounted for the assumption that 10% of participants would either not respond or have incomplete data.
2.6. Statistical analysis
Data were entered electronically using the IBM Statistical Package for the Social Sciences (SPSS) for Windows (Version 22.0; SPSS Inc., New York, NY). The proportions were expressed as frequencies (%). Continuous data, such as age and BMI, were evaluated for normality using the Shapiro–Wilk test and found to be non-normally distributed. The non-normally distributed data were expressed as median (interquartile range [IQR]). A univariate binary analysis was performed with H. pylori seropositivity as the dependent variable and age, sex, parental educational level and occupation, BMI, and adolescents’ mode of delivery as independent variables. Thereafter, all variables with a p-value of < 0.2 were included in a multivariable binary analysis to identify independently associated factors, while controlling for potential confounders. The adjusted odds ratios (AORs) and 95% confidence intervals (CIs) were calculated accordingly. A two-sided p-value of < 0.05 was considered statistically significant.
3. Results
Of the 235 adolescents recruited, 124 (52.8%) were males, and 111 (47.2%) were females. The median (IQR) age of the total sample was 14.0 (12.0‒16.0) years, and the median (IQR) BMI of the total sample was 16.2 (14.7‒18.4) kg/m2. The median (IQR) number of family members in the total sample was 7 (6‒9). Of the 235 participants, 39 (16.6%) had mothers, and 62 (26.4%) had fathers with at least a secondary education. Nearly one in ten mothers (8.9%) were employed. Among all participants, 209 (88.9%) reported that their fathers were employed.
The majority of adolescents and their families were displaced to northern Sudan, 108 (46.0%), followed by Khartoum, 95 (40.0%), and eastern Sudan, 32 (13.6%). Of the total participants, the majority were delivered vaginally, 225 (95.7%), while the rest were delivered by caesarean section, 10 (4.3%). Only a few adolescents used tobacco, 4 (1.7%).
The overall prevalence of H. pylori seropositivity was 24.7%. In the univariate analysis, adolescents’ mode of delivery was associated with H. pylori seropositivity, while age, sex, number of family members, BMI, parental education and occupation, and displacement were not associated with H. pylori seropositivity (Table 1).
Table 1.
Univariate binary analysis of the factors associated with H. pyloriin adolescents in central Sudan (n = 235), 2025.
| Variable | Total (n = 235) | Adolescents withhelicobacter pylori(n = 58) | Adolescents withouthelicobacter pylori(n = 177) | Odds ratio (95% confidence interval) | P value | |
|---|---|---|---|---|---|---|
| Median (Interquartile range) | ||||||
| Age (years) | 14.0 (12.0‒16.0) | 14.0 (12.0‒17.0) | 14.0 (12.0‒16.0) | 1.09 (0.97‒1.23) | 0.115 | |
| Number of family members | 7(6‒9) | 7 (6‒8) | 7 (6‒9) | 0.88 (0.77‒1.01) | 0.068 | |
| Body mass index (kg/m2) | 16.2 (14.7‒18.4) | 16.5 (14.8‒19.8) | 16.1 (14.6‒17.6) | 1.04 (0.97‒1.12) | 0.241 | |
| Frequency (proportion) | ||||||
| Sex | Male | 124 (52.8) | 26 (44.8) | 98 (55.4) | Reference | 0.164 |
| Female | 111 (47.2) | 32 (55.2) | 79 (44.6) | 1.52 (0.84‒2.77) | ||
| Mother Education | ≥secondary | 39 (16.6) | 8 (13.8) | 31 (17.5) | Reference | 0.510 |
| <secondary | 196 (83.4) | 50 (86.2) | 146 (82.5) | 0.75 (0.32‒1.74) | ||
| Father education | ≥secondary | 62 (26.4) | 16 (27.6) | 46 (26.0) | Reference | 0.811 |
| <secondary | 173 (73.6) | 42 (72.4) | 131 (74.0) | 0.92 (0.47‒1.79) | ||
| Mother occupation | Employed | 21 (8.9) | 8 (13.8) | 13 (7.3) | Reference | 0.141 |
| House wife | 214 (91.1) | 50 (86.2) | 164 (92.7) | 0.49 (0.19‒1.26) | ||
| Father occupation | Employed | 209 (88.9) | 53 (91.4) | 156 (88.1) | Reference | 0.496 |
| Unemployed | 26 (11.1) | 5 (8.6) | 21 (11.9) | 0.70 (0.25‒1.95) | ||
| Displacement area | Eastern Sudan | 32 (13.6) | 10 (17.2) | 22 (12.4) | Reference | |
| Northern Sudan | 108 (46.0) | 24 (41.4) | 84 (47.5) | 0.62 (0.26‒1.50) | 0.298 | |
| Khartoum | 95 (40.4) | 24 (41.4) | 71 (40.1) | 0.74 (0.30‒1.79) | 0.509 | |
| Adolescents’ mode of delivery | Vaginal | 225 (95.7) | 52 (89.7) | 173 (97.7) | Reference | |
| Caesarean section | 10 (4.3) | 6 (10.3) | 4 (2.3) | 4.99 (1.35‒18.35) | 0.016 | |
In the multivariable regression analysis, only adolescents’ mode of delivery was associated with H. pylori seropositivity (AOR = 3.97; 95% CI: 1.04‒15.18; Table 2).
Table 2.
Multivariable logistic regression analysis of factors associated with Helicobacter pyloriin adolescents in central Sudan (number = 235), 2025).
| Variable | Odds ratio (95% confidence interval) | P value | |
|---|---|---|---|
| Age (years) | 1.10 (0.97‒1.25) | 0.118 | |
| Number of family members | 0.87 (0.76‒1.01) | 0.079 | |
| Sex | Male | Reference | 0.599 |
| Female | 1.19 (0.62‒2.27) | ||
| Mother occupation | Employed | Reference | 0.200 |
| House wife | 0.52 (0.19‒1.40) | ||
| Adolescents’ mode of delivery | Vaginal | Reference | 0.044 |
| Caesarean section | 3.97 (1.04‒15.18) | ||
4. Discussion
The primary finding of the present study was that 24.7% of adolescents in Central Sudan were H. pylori seropositive. This prevalence of H. pylori seropositivity (24.7%) is similar to that reported in eastern Sudan [15]. A study in eastern Sudan included 431 school children (aged 8–18 years) and found that 21.8% of them were H. pylori seropositive [15]. By contrast, the prevalence rate (24.7%) of H. pylori seropositivity in this study is higher than previously reported rates in various African countries, including Sudan [16,19,24]. The authors’ previous research revealed a prevalence rate of H. pylori seropositivity among adolescents in northern Sudan of 8.4%. A study from Tanzania included 200 children aged 6 months to 17 years, of whom 11.5% were found to have H. pylori [19]. Moreover, in Ghana, a cross-sectional study included 240 asymptomatic children aged 7–16 years and reported an H. pylori prevalence of 14.2% [16]. The prevalence of H. pylori in this study was lower than that previously reported in Ethiopia (65.7%) [14] and Nigeria (32.8%) [17].
Data from a recent systematic review and meta-analysis that included 198 studies with a total of 152,650 children aged 18 years or younger indicated an overall global prevalence of H. pylori infection in children of 32.3%. The prevalence was higher in LMICs than high-income countries (HICs; 43·2% vs. 21·7%) [8].
The higher prevalence in this study compared to other studies, including those in northern Sudan, could be explained by the displacement conditions [24].
In this study, sociodemographic factors such as age, gender, BMI, family size, parent education, and occupation were investigated and found not to be associated with H. pylori seropositivity. This aligns with findings from other studies that have also revealed no significant associations between H. pylori and factors such as age [2,15,20,24], parental educational status [16], gender [20,37], BMI [24], and family size [2] in adolescents. Interestingly, traditional risk factors for H. pylori seropositivity, including age, sex, number of family members, BMI, parental education and occupation, and displacement status, were not significantly associated with H. pylori seropositivity in this study. This contrasts with certain studies in which socioeconomic status, household crowding, and poor hygiene are frequently cited as major determinants of H. pylori prevalence, particularly in endemic regions [14–16,18–20,24,37]. These factors have been reported in various studies, including in Sudan, indicating an association between H. pylori seropositivity and age [14,18,19], gender [16,24,38], BMI [15], family size [19], parent education and occupation [19,20]. The absence of any association with these factors in this study may suggest that in a highly endemic community such as Central Sudan, exposure to H. pylori is widespread, potentially leading to a saturation effect where these factors no longer differentiate risk as significantly. Conversely, characteristics specific to the asymptomatic adolescent cohort, or the community-based nature of this study, could also influence these observations. The displacement status, while not directly associated, could indirectly contribute to the overall high prevalence of H. pylori seropositivity through disrupted sanitation and living conditions. However, the widespread exposure might mask its effect.
This study reported that the mode of delivery, specifically caesarean section, is significantly associated with a higher likelihood of H. pylori seropositivity among asymptomatic adolescents in Central Sudan. This finding is a novel and important contribution to the literature. The association (AOR = 3.97; 95% CI: 1.04–15.18) suggests that early-life exposures may play a critical role in long-term susceptibility to infection, even in a high-prevalence setting.
This finding aligns with a growing body of evidence linking caesarean section to an increased risk of various non-communicable and infectious diseases in later life. As mentioned above in the introduction, the mode of delivery significantly influences the initial colonisation of the infant’s gut microbiome [28,32]. Infants born vaginally are exposed to the mother’s vaginal and faecal microbiota, which is rich in beneficial bacteria such as Lactobacillus and Bifidobacterium. By contrast, caesarean-born infants are first colonised by microbes from the hospital environment and the mother’s skin, often leading to a less diverse and distinct gut microbial community [38].
The early establishment of a diverse and stable gut microbiome is crucial for the proper maturation of the immune system [27,34,35]. It is hypothesised that this initial ‘microbial education’ trains the host’s immune system, promoting tolerance and an effective response against pathogens. A compromised or delayed gut microbiota development, as observed in infants delivered via caesarean section, may result in an altered immune system, leaving the individual more vulnerable to infectious agents such as H. pylori throughout childhood and adolescence. A recent meta-analysis demonstrated a link between caesarean section and increased risk of hospital admission for respiratory and gastrointestinal infections in children [29]. This study goes further by pinpointing an association with H. pylori acquisition.
Although there are a few direct studies specifically linking caesarean section to H. pylori infection in adolescents, the authors can infer potential long-term impacts based on current understanding of the gut microbiome and H. pylori transmission. In summary, while caesarean section does not directly cause H. pylori infection, it can lead to an altered early gut microbiome. This altered microbiome, in turn, may influence an adolescent's susceptibility to H. pylori infection or the long-term consequences of such an infection by impacting immune development and gut health. More targeted research is recommended to fully clarify this potential long-term impact.
These results should be carefully compared with the results of other studies. First, there may be differences in inclusion and exclusion criteria. For example, this study screened asymptomatic adolescents from the community, while other studies included adolescents with gastrointestinal symptoms in a hospital-based setting. Second, while the present study used the WHO cut-off age of 10–19 years, other studies used different age ranges for adolescents (early adolescent, late adolescent, or both adolescent and children). Third, various tests have been used to detect H. pylori. These differences in prevalence and risk factors within and between countries highlight the need for further research on H. pylori.
The findings have significant implications for public health. With the high prevalence of H. pylori in asymptomatic adolescents and the potential long-term health risks, these results highlight the importance of considering screening strategies in high-risk populations. In addition, the association identified with mode of delivery suggests a new direction for research into early-life interventions that could reduce the risk of H. pylori acquisition.
4.1. Strengths and limitations
The present study has several strengths, including its community-based design, which provides a more representative prevalence of H. pylori seropositivity among asymptomatic adolescents and avoids the selection bias of hospital-based studies. A key strength is the novel investigation of mode of delivery as a potential risk factor, making a unique contribution to the literature. The use of multivariate analysis adds credibility to the finding that caesarean section is significantly associated with infection. However, the study also has certain limitations that need to be acknowledged in order to improve future research. Its cross-sectional design precludes the establishment of causality; therefore, the authors cannot definitively conclude that the mode of delivery directly causes H. pylori infection. Longitudinal studies are recommended to understand the temporal relationship. The association is based on only 10 participants delivered by caesarean section, resulting in a wide confidence interval and limited statistical precision. Therefore, this finding should be presented as exploratory and hypothesis-generating rather than as evidence of an independent risk factor. Also, excluding only ‘healthy’ participants may introduce bias. Additionally, the use of a rapid serological antibody test represents an important limitation because it cannot distinguish between active infection and previous exposure. Consequently, the reported prevalence more accurately reflects H. pylori seropositivity than confirmed active infection. The observed association may be influenced by unmeasured confounding factors, including residual confounding such as maternal H. pylori status, breastfeeding practices, antibiotic exposure during infancy, childhood socioeconomic conditions, sanitation, and indications for caesarean delivery. Furthermore, the study was conducted in a specific region of Central Sudan, which limits the generalisability of its results to other populations or areas with different epidemiological contexts.
5. Conclusions
The present study reveals a significant prevalence of H. pylori seropositivity among asymptomatic adolescents in Central Sudan. Because the association is based on only 10 participants delivered by caesarean section, the confidence interval is wide and statistical precision is limited. Therefore, this finding should be presented as exploratory and hypothesis-generating rather than as evidence of an independent risk factor. Given the cross-sectional design and methodological limitations, the study demonstrates an association only, and prospective longitudinal studies using more accurate diagnostic methods are needed to confirm these findings. It is essential to expand research to other regions of Sudan and investigate the clinical outcomes of asymptomatic infection in this population. In addition, further research, potentially involving gut microbiome analysis, is needed to fully elucidate this mechanism.
Acknowledgements
The Researchers would like to thank the Deanship of Graduate Studies and Scientific Research at Qassim University (https://www.qu.edu.sa) for financial support (QU-APC-2026). The authors would like to thank all participants and their guardians for their valuable contribution to this study. The authors also extend their gratitude to the research assistants for their diligent work in data collection.
Author contributions
WMA, ASA, and AA: Conceptualisation, Methodology, Formal Analysis, Writing—Original Draft, Writing—Review & Editing. WMA, ASA, and IA: Data Curation, Investigation. ASA and IA: Supervision. All authors read and approved the final manuscript.
Disclosure statement
No potential conflict of interest was reported by the author(s).
Funding
This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
Data availability statement
The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.
Ethical considerations
The study protocol was approved by the Institutional Review Board (IRB) of the Faculty of Medicine and Health Sciences at the University of Gadarif in Gadarif, eastern Sudan (Ref. #2025, 04). Informed written consent was obtained from all participants and their legal guardians before data collection. Participants were assured of confidentiality and anonymity. They were informed that participation was voluntary and they had the right to withdraw at any time without penalty. Referrals to the nearest health services for further evaluation and management, if needed, were provided for participants identified with seropositive H. pylori.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.